Repression of BIM mediates survival signaling by MYC and AKT in high-risk T-cell acute lymphoblastic leukemia

Leukemia

Volumn 28, Issue 9, 2014, Pages 1819-1827

  Reynolds, C ^a   Roderick, J E ^b   LaBelle, J L ^a,c,d   Bird, G ^c   Mathieu, R ^a   Bodaar, K ^a   Colon, D ^c   Pyati, U ^c   Stevenson, K E ^e   Qi, J ^e   Harris, M ^a   Silverman, L B ^a,c   Sallan, S E ^a,c   Bradner, J E ^e   Neuberg, D S ^e   Look, A T ^a,c   Walensky, L D ^a,c   Kelliher, M A ^b   Gutierrez, A ^a,c  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^c DANA FARBER CANCER INSTITUTE   (United States)

^d UNIVERSITY OF CHICAGO   (United States)

^e HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIM PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B;

ACUTE LYMPHOBLASTIC LEUKEMIA; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER SURVIVAL; CONTROLLED STUDY; DOWN REGULATION; HETEROZYGOTE; HUMAN; HUMAN CELL; MOLECULAR PATHOLOGY; MOUSE; NONHUMAN; ONCOGENE MYC; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; T CELL ACUTE LYMPHOBLASTIC LEUKEMIA; T LYMPHOBLAST; UPREGULATION; ZEBRA FISH;

ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; CELL LINE, TUMOR; HUMANS; IMIDAZOLES; MEMBRANE PROTEINS; MICRORNAS; PHOSPHATIDYLINOSITOL 3-KINASES; PRECURSOR T-CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; PROTO-ONCOGENE PROTEINS C-MYC; QUINOLINES; SIGNAL TRANSDUCTION; ZEBRAFISH;

EID: 84908303875     PISSN: 08876924     EISSN: 14765551     Source Type: Journal    
DOI: 10.1038/leu.2014.78     Document Type: Article

References (49)

1. Gutierrez A, Sanda T, Grebliunaite R, Carracedo A, Salmena L, Ahn Y., et al. High frequency of PTEN, PI3K, and AKT abnormalities in T-cell acute lymphoblastic leukemia. Blood. 2009; 114: 647-650
2. Gutierrez A, Dahlberg SE, Neuberg DS, Zhang J, Grebliunaite R, Sanda T., et al. Absence of biallelic TCRgamma deletion predicts early treatment failure in pediatric T-cell acute lymphoblastic leukemia. J Clin Oncol. 2010; 28: 3816-3823
3. Zhang J, Ding L, Holmfeldt L, Wu G, Heatley SL, Payne-Turner D., et al. The genetic basis of early T-cell precursor acute lymphoblastic leukaemia. Nature. 2012; 481: 157-163
4. Weng AP, Ferrando AA, Lee W, JPt Morris, Silverman LB, Sanchez-Irizarry C., et al. Activating mutations of NOTCH1 in human T cell acute lymphoblastic leukemia. Science. 2004; 306: 269-271
5. Sharma VM, Calvo JA, Draheim KM, Cunningham LA, Hermance N, Beverly L., et al. Notch1 contributes to mouse T-cell leukemia by directly inducing the expression of c-myc. Mol Cell Biol. 2006; 26: 8022-8031
6. Palomero T, Lim WK, Odom DT, Sulis ML, Real PJ, Margolin A., et al. NOTCH1 directly regulates c-MYC and activates a feed-forward-loop transcriptional network promoting leukemic cell growth. Proc Natl Acad Sci USA. 2006; 103: 18261-18266
7. Weng AP, Millholland JM, Yashiro-Ohtani Y, Arcangeli ML, Lau A, Wai C., et al. c-Myc is an important direct target of Notch1 in T-cell acute lymphoblastic leukemia/ lymphoma. Genes Dev. 2006; 20: 2096-2109
8. Hebert J, Cayuela JM, Berkeley J, Sigaux F. Candidate tumor-suppressor genes MTS1 (p16INK4A) and MTS2 (p15INK4B) display frequent homozygous deletions in primary cells from T- but not from B-cell lineage acute lymphoblastic leukemias. Blood. 1994; 84: 4038-4044
9. Van Vlierberghe P, Ferrando A. The molecular basis of T cell acute lymphoblastic leukemia. J Clin Invest. 2012; 122: 3398-3406
10. Gutierrez A, Grebliunaite R, Feng H, Kozakewich E, Zhu S, Guo F., et al. Pten mediates Myc oncogene dependence in a conditional zebrafish model of T cell acute lymphoblastic leukemia. J Exp Med. 2011; 208: 1595-1603
11. Palomero T, Sulis ML, Cortina M, Real PJ, Barnes K, Ciofani M., et al. Mutational loss of PTEN induces resistance to NOTCH1 inhibition in T-cell leukemia. Nat Med. 2007; 13: 1203-1210
12. Subramaniam PS, Whye DW, Efimenko E, Chen J, Tosello V, De Keersmaecker K., et al. Targeting nonclassical oncogenes for therapy in T-ALL. Cancer Cell. 2012; 21: 459-472
13. Bouillet P, Purton JF, Godfrey DI, Zhang LC, Coultas L, Puthalakath H., et al. BH3-only Bcl-2 family member Bim is required for apoptosis of autoreactive thymocytes. Nature. 2002; 415: 922-926
14. Bouillet P, Metcalf D, Huang DC, Tarlinton DM, Kay TW, Kontgen F., et al. Proapoptotic Bcl-2 relative Bim required for certain apoptotic responses, leukocyte homeostasis, and to preclude autoimmunity. Science. 1999; 286: 1735-1738
15. Ryan JA, Brunelle JK, Letai A. Heightened mitochondrial priming is the basis for apoptotic hypersensitivity of CD4+ CD8+ thymocytes. Proc Natl Acad Sci USA. 2010; 107: 12895-12900
16. Bassing CH, Swat W, Alt FW. The mechanism and regulation of chromosomal V(D)J recombination. Cell. 2002; 109(Suppl): S45-S55
17. Viret C, Janeway Jr. CA. MHC and T cell development. Rev Immunogenet. 1999; 1: 91-104
18. Langenau DM, Jette C, Berghmans S, Palomero T, Kanki JP, Kutok JL., et al. Suppression of apoptosis by bcl-2 overexpression in lymphoid cells of transgenic zebrafish. Blood. 2005; 105: 3278-3285
19. Golling G, Amsterdam A, Sun Z, Antonelli M, Maldonado E, Chen W., et al. Insertional mutagenesis in zebrafish rapidly identifies genes essential for early vertebrate development. Nat Genet. 2002; 31: 135-140
20. Filippakopoulos P, Qi J, Picaud S, Shen Y, Smith WB, Fedorov O., et al. Selective inhibition of BET bromodomains. Nature. 2010; 468: 1067-1073
21. Rakhra K, Bachireddy P, Zabuawala T, Zeiser R, Xu L, Kopelman A., et al. CD4(+) T cells contribute to the remodeling of the microenvironment required for sustained tumor regression upon oncogene inactivation. Cancer Cell. 2010; 18: 485-498
22. Gutierrez A, Sanda T, Ma W, Zhang J, Grebliunaite R, Dahlberg S., et al. Inactivation of LEF1 in T-cell acute lymphoblastic leukemia. Blood. 2010; 115: 2845-2851
23. O'Neil J, Grim J, Strack P, Rao S, Tibbitts D, Winter C., et al. FBW7 mutations in leukemic cells mediate NOTCH pathway activation and resistance to gammasecretase inhibitors. J Exp Med. 2007; 204: 1813-1824
24. LaBelle JL, Katz SG, Bird GH, Gavathiotis E, Stewart ML, Lawrence C., et al. A stapled BIM peptide overcomes apoptotic resistance in hematologic cancers. J Clin Invest. 2012; 122: 2018-2031
25. Nakae J, Barr V, Accili D. Differential regulation of gene expression by insulin and IGF-1 receptors correlates with phosphorylation of a single amino acid residue in the forkhead transcription factor FKHR. EMBO. J. 2000; 19: 989-996
26. Davids MS, Letai A. Targeting the B-cell lymphoma/leukemia 2 family in cancer. J Clin Oncol. 2012; 30: 3127-3135
27. Jette CA, Flanagan AM, Ryan J, Pyati UJ, Carbonneau S, Stewart RA., et al. BIM and other BCL-2 family proteins exhibit cross-species conservation of function between zebrafish and mammals. Cell Death Differ. 2008; 15: 1063-1072
28. Maira SM, Stauffer F, Brueggen J, Furet P, Schnell C, Fritsch C., et al. Identification and characterization of NVP-BEZ235, a new orally available dual phosphatidylinositol 3-kinase/mammalian target of rapamycin inhibitor with potent in vivo antitumor activity. Mol Cancer Ther. 2008; 7: 1851-1863
29. Delmore JE, Issa GC, Lemieux ME, Rahl PB, Shi J, Jacobs HM., et al. BET bromodomain inhibition as a therapeutic strategy to target c-Myc. Cell. 2011; 146: 904-917
30. Wei G, Twomey D, Lamb J, Schlis K, Agarwal J, Stam RW., et al. Gene expressionbased chemical genomics identifies rapamycin as a modulator of MCL1 and glucocorticoid resistance. Cancer Cell. 2006; 10: 331-342
31. Maurer U, Charvet C, Wagman AS, Dejardin E, Green DR. Glycogen synthase kinase-3 regulates mitochondrial outer membrane permeabilization and apoptosis by destabilization of MCL-1. Mol Cell. 2006; 21: 749-760
32. Manning BD, Cantley LC. AKT/PKB signaling: navigating downstream. Cell. 2007; 129: 1261-1274
33. Stahl M, Dijkers PF, Kops GJ, Lens SM, Coffer PJ, Burgering BM., et al. The forkhead transcription factor FoxO regulates transcription of p27Kip1 and Bim in response to IL-2. J Immunol. 2002; 168: 5024-5031
34. O'Donnell KA, Wentzel EA, Zeller KI, Dang CV, Mendell JT. c-Myc-regulated microRNAs modulate E2F1 expression. Nature. 2005; 435: 839-843
35. Mavrakis KJ, Wolfe AL, Oricchio E, Palomero T, de Keersmaecker K, McJunkin K., et al. Genome-wide RNA-mediated interference screen identifies miR-19 targets in Notch-induced T-cell acute lymphoblastic leukaemia. Nat Cell Biol. 2010; 12: 372-379
36. Gavathiotis E, Suzuki M, Davis ML, Pitter K, Bird GH, Katz SG., et al. BAX activation is initiated at a novel interaction site. Nature. 2008; 455: 1076-1081
37. Flicek P, Ahmed I, Amode MR, Barrell D, Beal K, Brent S., et al. Ensembl 2013. Nucleic Acids Res. 2013; 41: D48-D55
38. O'Connor L, Strasser A, O'Reilly LA, Hausmann G, Adams JM, Cory S., et al. Bim: a novel member of the Bcl-2 family that promotes apoptosis. EMBO. J. 1998; 17: 384-395
39. Liu JW, Chandra D, Tang SH, Chopra D, Tang DG. Identification and characterization of Bimgamma, a novel proapoptotic BH3-only splice variant of Bim. Cancer Res. 2002; 62: 2976-2981
40. Marani M, Tenev T, Hancock D, Downward J, Lemoine NR. Identification of novel isoforms of the BH3 domain protein Bim which directly activate Bax to trigger apoptosis. Mol Cell Biol. 2002; 22: 3577-3589
41. Hemann MT, Bric A, Teruya-Feldstein J, Herbst A, Nilsson JA, Cordon-Cardo C., et al. Evasion of the p53 tumour surveillance network by tumour-derived MYC mutants. Nature. 2005; 436: 807-811
42. Sherr CJ. Divorcing ARF and p53: an unsettled case. Nat Rev Cancer. 2006; 6: 663-673
43. Gutierrez A, Feng H, Stevenson K, Neuberg DS, Calzada O, Zhou Y., et al. Loss of function tp53 mutations do not accelerate the onset of Myc-induced T-ALL in the zebrafish. Br J Haematol (in press
44. Chonghaile TN, Sarosiek KA, Vo TT, Ryan JA, Tammareddi A, Moore VD., et al. Pretreatment mitochondrial priming correlates with clinical response to cytotoxic chemotherapy. Science. 2011; 334: 1129-1133
45. Deng J, Carlson N, Takeyama K, Dal Cin P, Shipp M, Letai A. BH3 profiling identifies three distinct classes of apoptotic blocks to predict response to ABT-737 and conventional chemotherapeutic agents. Cancer Cell. 2007; 12: 171-185
46. Vo TT, Ryan J, Carrasco R, Neuberg D, Rossi DJ, Stone RM., et al. Relative mitochondrial priming of myeloblasts and normal HSCs determines chemotherapeutic success in AML. Cell. 2012; 151: 344-355
47. Bachmann PS, Piazza RG, Janes ME, Wong NC, Davies C, Mogavero A., et al. Epigenetic silencing of BIM in glucocorticoid poor-responsive pediatric acute lymphoblastic leukemia, and its reversal by histone deacetylase inhibition. Blood. 2010; 116: 3013-3022
48. Happo L, Cragg MS, Phipson B, Haga JM, Jansen ES, Herold MJ., et al. Maximal killing of lymphoma cells by DNA damage-inducing therapy requires not only the p53 targets Puma and Noxa, but also Bim. Blood. 2010; 116: 5256-5267
49. Richter-Larrea JA, Robles EF, Fresquet V, Beltran E, Rullan AJ, Agirre X., et al. Reversion of epigenetically mediated BIM silencing overcomes chemoresistance in Burkitt lymphoma. Blood. 2010; 116: 2531-2542